1932

Abstract

The molecular and genetic basis for the evolution of anatomical diversity is a major question that has inspired evolutionary and developmental biologists for decades. Because morphology takes form during development, a true comprehension of how anatomical structures evolve requires an understanding of the evolutionary events that alter developmental genetic programs. Vast gene regulatory networks (GRNs) that connect transcription factors to their target regulatory sequences control gene expression in time and space and therefore determine the tissue-specific genetic programs that shape morphological structures. In recent years, many new examples have greatly advanced our understanding of the genetic alterations that modify GRNs to generate newly evolved morphologies. Here, we review several aspects of GRN evolution, including their deep preservation, their mechanisms of alteration, and how they originate to generate novel developmental programs.

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2015-08-24
2024-04-17
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Literature Cited

  1. Abouheif E. 1.  1999. Establishing homology criteria for regulatory gene networks: prospects and challenges. Novartis Found. Symp. 222:207–21; discussion 222–25 [Google Scholar]
  2. Adegbola AA, Cox GF, Bradshaw EM, Hafler DA, Gimelbrant A, Chess A. 2.  2015. Monoallelic expression of the human FOXP2 speech gene. PNAS 1126848–54
  3. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V. 3.  et al. 2007. Deletion of ultraconserved elements yields viable mice. PLOS Biol. 5:e234 [Google Scholar]
  4. Akbari OS, Bae E, Johnsen H, Villaluz A, Wong D, Drewell RA. 4.  2008. A novel promoter-tethering element regulates enhancer-driven gene expression at the bithorax complex in the Drosophila embryo. Development 135:123–31 [Google Scholar]
  5. Alon U. 5.  2007. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 8:450–61 [Google Scholar]
  6. Alvarez AD, Shi W, Wilson BA, Skeath JB. 6.  2003. pannier and pointedP2 act sequentially to regulate Drosophila heart development. Development 130:3015–26 [Google Scholar]
  7. Arnoult L, Su KFY, Manoel D, Minervino C, Magrina J. 7.  et al. 2013. Emergence and diversification of fly pigmentation through evolution of a gene regulatory module. Science 339:1423–26 [Google Scholar]
  8. Averof M, Patel NH. 8.  1997. Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388:682–86 [Google Scholar]
  9. Avery L, Wasserman S. 9.  1992. Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet. 8:312–16 [Google Scholar]
  10. Babbitt CC, Fedrigo O, Pfefferle AD, Boyle AP, Horvath JE. 10.  et al. 2010. Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain. Genome Biol. Evol. 2:67–79 [Google Scholar]
  11. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR. 11.  et al. 2009. Diversity and complexity in DNA recognition by transcription factors. Science 324:1720–23 [Google Scholar]
  12. Baltimore D. 12.  2001. Our genome unveiled. Nature 409:814–16 [Google Scholar]
  13. Barolo S, Posakony JW. 13.  2002. Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev. 16:1167–81 [Google Scholar]
  14. Baxter SW, Papa R, Chamberlain N, Humphray SJ, Joron M. 14.  et al. 2008. Convergent evolution in the genetic basis of Müllerian mimicry in Heliconius butterflies. Genetics 180:1567–77 [Google Scholar]
  15. Bejerano G, Lowe CB, Ahituv N, King B, Siepel A. 15.  et al. 2006. A distal enhancer and an ultraconserved exon are derived from a novel retroposon. Nature 441:87–90 [Google Scholar]
  16. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW III, Bulyk ML. 16.  2006. Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat. Biotechnol. 24:1429–35 [Google Scholar]
  17. Black BL, Olson EN. 17.  1998. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 14:167–96 [Google Scholar]
  18. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y. 18.  2010. Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 20:180–89 [Google Scholar]
  19. Bodmer R. 19.  1993. The gene tinman is required for specification of the heart and visceral muscles in Drosophila. Development 118:719–29 [Google Scholar]
  20. Brayer KJ, Lynch VJ, Wagner GP. 20.  2011. Evolution of a derived protein-protein interaction between HoxA11 and Foxo1a in mammals caused by changes in intramolecular regulation. PNAS 108:E414–20 [Google Scholar]
  21. Bridges CB, Morgan TH. 21.  1919. The second chromosome group of mutant characters. Contributions to the Genetics of Drosophila melanogaster by CB Bridges, TH Morgan, AH Sturtevant 123–304 Carnegie Inst. Wash. Publ. 278 Washington, DC: Carnegie Inst. Wash. [Google Scholar]
  22. Bridges CB, Morgan TH. 22.  1923. The Third-Chromosome Group of Mutant Characters of Drosophila melanogaster Carnegie Inst. Wash. Publ. 327 Washington, DC: Carnegie Inst. Wash.
  23. Britten RJ, Davidson EH. 23.  1969. Gene regulation for higher cells: a theory. Science 165:349–57 [Google Scholar]
  24. Burgess-Beusse B, Farrell C, Gaszner M, Litt M, Mutskov V. 24.  et al. 2002. The insulation of genes from external enhancers and silencing chromatin. PNAS 99:Suppl. 416433–37 [Google Scholar]
  25. Calhoun VC, Stathopoulos A, Levine M. 25.  2002. Promoter-proximal tethering elements regulate enhancer-promoter specificity in the Drosophila Antennapedia complex. PNAS 99:9243–47 [Google Scholar]
  26. Campbell G, Weaver T, Tomlinson A. 26.  1993. Axis specification in the developing Drosophila appendage: the role of wingless, decapentaplegic, and the homeobox gene aristaless. Cell 74:1113–23 [Google Scholar]
  27. Cande JD, Chopra VS, Levine M. 27.  2009. Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum. Development 136:3153–60 [Google Scholar]
  28. Carbone MA, Llopart A, deAngelis M, Coyne JA, Mackay TF. 28.  2005. Quantitative trait loci affecting the difference in pigmentation between Drosophila yakuba and D. santomea. Genetics 171:211–25 [Google Scholar]
  29. Carroll SB, Grenier JK, Weatherbee SD. 29.  2005. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design Malden, MA: Blackwell, 2nd ed..
  30. Carroll SB, Scott MP. 30.  1986. Zygotically active genes that affect the spatial expression of the fushi tarazu segmentation gene during early Drosophila embryogenesis. Cell 45:113–26 [Google Scholar]
  31. Chan YF, Marks ME, Jones FC, Villarreal G Jr, Shapiro MD. 31.  et al. 2010. Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327:302–5 [Google Scholar]
  32. Cheatle Jarvela AM, Brubaker L, Vedenko A, Gupta A, Armitage BA. 32.  et al. 2014. Modular evolution of DNA-binding preference of a Tbrain transcription factor provides a mechanism for modifying gene regulatory networks. Mol. Biol. Evol. 31:2672–88 [Google Scholar]
  33. Chen L, Zhao P, Wells L, Amemiya CT, Condie BG, Manley NR. 33.  2010. Mouse and zebrafish Hoxa3 orthologues have nonequivalent in vivo protein function. PNAS 107:10555–60 [Google Scholar]
  34. Chung H, Bogwitz MR, McCart C, Andrianopoulos A, Ffrench-Constant RH. 34.  et al. 2007. Cis-regulatory elements in the Accord retrotransposon result in tissue-specific expression of the Drosophila melanogaster insecticide resistance gene Cyp6g1. Genetics 175:1071–77 [Google Scholar]
  35. Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G Jr, Dickson M. 35.  et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles. Science 307:1928–33 [Google Scholar]
  36. Cotney J, Leng J, Yin J, Reilly SK, DeMare LE. 36.  et al. 2013. The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154:185–96 [Google Scholar]
  37. Cripps RM, Olson EN. 37.  2002. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol. 246:14–28 [Google Scholar]
  38. Darwin C. 38.  1859. On the Origin of Species by Means of Natural Selection; or, The Preservation of Favoured Races in the Struggle for Life London: Murray
  39. Davidson EH. 39.  2001. Genomic Regulatory Systems: Development and Evolution San Diego, CA: Academic
  40. Davidson EH. 40.  2006. The Regulatory Genome: Gene Regulatory Networks in Development and Evolution San Diego, CA: Academic
  41. de Koning APJ, Gu W, Castoe TA, Batzer MA, Pollock DD. 41.  2011. Repetitive elements may comprise over two-thirds of the human genome. PLOS Genet. 7:e1002384 [Google Scholar]
  42. de Souza FSJ, Franchini LF, Rubinstein M. 42.  2013. Exaptation of transposable elements into novel cis-regulatory elements: Is the evidence always strong?. Mol. Biol. Evol. 30:1239–51 [Google Scholar]
  43. de-Leon SB-T, Davidson EH. 43.  2010. Information processing at the foxa node of the sea urchin endomesoderm specification network. PNAS 107:10103–8 [Google Scholar]
  44. Domené S, Bumaschny VF, de Souza FSJ, Franchini LF, Nasif S. 44.  et al. 2013. Enhancer turnover and conserved regulatory function in vertebrate evolution. Philos. Trans. R. Soc. Lond. B. 368:20130027 [Google Scholar]
  45. Eichenlaub MP, Ettwiller L. 45.  2011. De novo genesis of enhancers in vertebrates. PLOS Biol. 9e1001188
  46. Emlen DJ, Szafran Q, Corley LS, Dworkin I. 46.  2006. Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle “horns.”. Heredity 97:179–91 [Google Scholar]
  47. Enard W, Gehre S, Hammerschmidt K, Hölter SM, Blass T. 47.  et al. 2009. A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137:961–71 [Google Scholar]
  48. Enard W, Przeworski M, Fisher SE, Lai CSL, Wiebe V. 48.  et al. 2002. Molecular evolution of Foxp2, a gene involved in speech and language. Nature 418:869–72 [Google Scholar]
  49. Fedrigo O, Pfefferle AD, Babbitt CC, Haygood R, Wall CE, Wray GA. 49.  2011. A potential role for glucose transporters in the evolution of human brain size. Brain Behav. Evol. 78:315–26 [Google Scholar]
  50. Feschotte C. 50.  2008. Transposable elements and the evolution of regulatory networks. Nat. Rev. Genet. 9:397–405 [Google Scholar]
  51. Frankel N, Erezyilmaz DF, McGregor AP, Wang S, Payre F, Stern DL. 51.  2011. Morphological evolution caused by many subtle-effect substitutions in regulatory DNA. Nature 474:598–603 [Google Scholar]
  52. Frankel N, Wang S, Stern DL. 52.  2012. Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution. PNAS 109:20975–79 [Google Scholar]
  53. Galant R, Carroll SB. 53.  2002. Evolution of a transcriptional repression domain in an insect Hox protein. Nature 415:910–13 [Google Scholar]
  54. Gallant JR, Imhoff VE, Martin A, Savage WK, Chamberlain NL. 54.  et al. 2014. Ancient homology underlies adaptive mimetic diversity across butterflies. Nat. Commun. 5:4817 [Google Scholar]
  55. Gao F, Davidson EH. 55.  2008. Transfer of a large gene regulatory apparatus to a new developmental address in echinoid evolution. PNAS 105:6091–96 [Google Scholar]
  56. Garrett-Engele CM, Siegal ML, Manoli DS, Williams BC, Li H, Baker BS. 56.  2002. intersex, a gene required for female sexual development in Drosophila, is expressed in both sexes and functions together with doublesex to regulate terminal differentiation. Development 129:4661–75 [Google Scholar]
  57. Gerhart J. 56a.  1999. 1998 Warkany lecture: signaling pathways in development. Teratology 60:226–39 [Google Scholar]
  58. Geyer PK, Corces VG. 57.  1987. Separate regulatory elements are responsible for the complex pattern of tissue-specific and developmental transcription of the yellow locus in Drosophila melanogaster. Genes Dev. 1:996–1004 [Google Scholar]
  59. Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB. 58.  2005. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature 433:481–87 [Google Scholar]
  60. Gottesman S. 59.  1984. Bacterial regulation: global regulatory networks. Annu. Rev. Genet. 18:415–41 [Google Scholar]
  61. Greer JM, Puetz J, Thomas KR, Capecchi MR. 60.  2000. Maintenance of functional equivalence during paralogous Hox gene evolution. Nature 403:661–65 [Google Scholar]
  62. Grens A, Mason E, Marsh JL, Bode HR. 61.  1995. Evolutionary conservation of a cell fate specification gene: the Hydra achaete-scute homolog has proneural activity in Drosophila. Development 121:4027–35 [Google Scholar]
  63. Halder G, Callaerts P, Gehring WJ. 62.  1995. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 267:1788–92 [Google Scholar]
  64. Hanks MC, Loomis CA, Harris E, Tong CX, Anson-Cartwright L. 63.  et al. 1998. Drosophila engrailed can substitute for mouse Engrailed1 function in mid-hindbrain, but not limb development. Development 125:4521–30 [Google Scholar]
  65. Harding K, Hoey T, Warrior R, Levine M. 64.  1989. Autoregulatory and gap gene response elements of the even-skipped promoter of Drosophila. EMBO J. 8:1205–12 [Google Scholar]
  66. Hines HM, Papa R, Ruiz M, Papanicolaou A, Wang C. 65.  et al. 2012. Transcriptome analysis reveals novel patterning and pigmentation genes underlying Heliconius butterfly wing pattern variation. BMC Genomics 13:288 [Google Scholar]
  67. Hinman VF, Nguyen AT, Cameron RA, Davidson EH. 66.  2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. PNAS 100:13356–61 [Google Scholar]
  68. Hong J-W, Hendrix DA, Levine MS. 67.  2008. Shadow enhancers as a source of evolutionary novelty. Science 321:1314 [Google Scholar]
  69. Imsland F, Feng C, Boije H, Bed'hom B, Fillon V. 68.  et al. 2012. The Rose-comb mutation in chickens constitutes a structural rearrangement causing both altered comb morphology and defective sperm motility. PLOS Genet. 8:e1002775 [Google Scholar]
  70. Jeong S, Rebeiz M, Andolfatto P, Werner T, True J, Carroll SB. 69.  2008. The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132:783–93 [Google Scholar]
  71. Jeong S, Rokas A, Carroll SB. 70.  2006. Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125:1387–99 [Google Scholar]
  72. Johnson JE, Birren SJ, Anderson DJ. 71.  1990. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346:858–61 [Google Scholar]
  73. Kapan DD, Flanagan NS, Tobler A, Papa R, Reed RD. 72.  et al. 2006. Localization of Müllerian mimicry genes on a dense linkage map of Heliconius erato. Genetics 173:735–57 [Google Scholar]
  74. Kawashima T, Kawashima S, Tanaka C, Murai M, Yoneda M. 73.  et al. 2009. Domain shuffling and the evolution of vertebrates. Genome Res. 19:1393–403 [Google Scholar]
  75. King MC, Wilson AC. 74.  1975. Evolution at two levels in humans and chimpanzees. Science 188:107–16 [Google Scholar]
  76. Klinedinst SL, Bodmer R. 75.  2003. Gata factor Pannier is required to establish competence for heart progenitor formation. Development 130:3027–38 [Google Scholar]
  77. Kojima T. 76.  2004. The mechanism of Drosophila leg development along the proximodistal axis. Dev. Growth Differ. 46:115–29 [Google Scholar]
  78. Komuro I, Izumo S. 77.  1993. Csx: a murine homeobox-containing gene specifically expressed in the developing heart. PNAS 90:8145–49 [Google Scholar]
  79. Kopp A, Graze RM, Xu S, Carroll SB, Nuzhdin SV. 78.  2003. Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163:771–87 [Google Scholar]
  80. Krause J, Lalueza-Fox C, Orlando L, Enard W, Green RE. 79.  et al. 2007. The derived FOXP2 variant of modern humans was shared with Neandertals. Curr. Biol. 17:1908–12 [Google Scholar]
  81. Lai CSL, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP. 80.  2001. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:519–23 [Google Scholar]
  82. Lai CSL, Gerrelli D, Monaco AP, Fisher SE, Copp AJ. 81.  2003. FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126:2455–62 [Google Scholar]
  83. Lettice LA, Horikoshi T, Heaney SJ, van Baren MJ, van der Linde HC. 82.  et al. 2002. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. PNAS 99:7548–53 [Google Scholar]
  84. Levine M. 83.  2010. Transcriptional enhancers in animal development and evolution. Curr. Biol. 20:R754–63 [Google Scholar]
  85. Lints TJ, Parsons LM, Hartley L, Lyons I, Harvey RP. 84.  1993. Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119:419–31 [Google Scholar]
  86. Liubicich DM, Serano JM, Pavlopoulos A, Kontarakis Z, Protas ME. 85.  et al. 2009. Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. PNAS 106:13892–96 [Google Scholar]
  87. Llopart A, Elwyn S, Lachaise D, Coyne JA. 86.  2002. Genetics of a difference in pigmentation between Drosophila yakuba and Drosophila santomea. Evolution 56:2262–77 [Google Scholar]
  88. Lowe CB, Bejerano G, Haussler D. 87.  2007. Thousands of human mobile element fragments undergo strong purifying selection near developmental genes. PNAS 104:8005–10 [Google Scholar]
  89. Ludwig MZ, Bergman C, Patel NH, Kreitman M. 88.  2000. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature 403:564–67 [Google Scholar]
  90. Lynch VJ, Leclerc RD, May G, Wagner GP. 89.  2011. Transposon-mediated rewiring of gene regulatory networks contributed to the evolution of pregnancy in mammals. Nat. Genet. 43:1154–59 [Google Scholar]
  91. Lynch VJ, Wagner GP. 90.  2008. Resurrecting the role of transcription factor change in developmental evolution. Evolution 62:2131–54 [Google Scholar]
  92. Macdonald PM, Ingham P, Struhl G. 91.  1986. Isolation, structure, and expression of even-skipped: a second pair-rule gene of Drosophila containing a homeo box. Cell 47:721–34 [Google Scholar]
  93. Malicki J, Schughart K, McGinnis W. 92.  1990. Mouse Hox-2.2 specifies thoracic segmental identity in Drosophila embryos and larvae. Cell 63:961–67 [Google Scholar]
  94. Maricic T, Günther V, Georgiev O, Gehre S, Curlin M. 93.  et al. 2013. A recent evolutionary change affects a regulatory element in the human FOXP2 gene. Mol. Biol. Evol. 30:844–52 [Google Scholar]
  95. Martin A, McCulloch KJ, Patel NH, Briscoe AD, Gilbert LE, Reed RD. 94.  2014. Multiple recent co-options of Optix associated with novel traits in adaptive butterfly wing radiations. EvoDevo 5:7 [Google Scholar]
  96. Martin A, Papa R, Nadeau NJ, Hill RI, Counterman BA. 95.  et al. 2012. Diversification of complex butterfly wing patterns by repeated regulatory evolution of a Wnt ligand. PNAS 109:12632–37 [Google Scholar]
  97. McCauley BS, Weideman EP, Hinman VF. 96.  2010. A conserved gene regulatory network subcircuit drives different developmental fates in the vegetal pole of highly divergent echinoderm embryos. Dev. Biol. 340:200–8 [Google Scholar]
  98. McCauley BS, Wright EP, Exner C, Kitazawa C, Hinman VF. 97.  2012. Development of an embryonic skeletogenic mesenchyme lineage in a sea cucumber reveals the trajectory of change for the evolution of novel structures in echinoderms. EvoDevo 3:17 [Google Scholar]
  99. McGregor AP, Orgogozo V, Delon I, Zanet J, Srinivasan DG. 98.  et al. 2007. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 448:587–90 [Google Scholar]
  100. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD. 99.  et al. 2011. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471:216–19 [Google Scholar]
  101. Moczek AP, Emlen D. 100.  2000. Male horn dimorphism in the scarab beetle, Onthophagus taurus: Do alternative reproductive tactics favour alternative phenotypes?. Anim. Behav. 59:459–66 [Google Scholar]
  102. Moczek AP, Nagy LM. 101.  2005. Diverse developmental mechanisms contribute to different levels of diversity in horned beetles. Evol. Dev. 7:175–85 [Google Scholar]
  103. Moczek AP, Rose DJ. 102.  2009. Differential recruitment of limb patterning genes during development and diversification of beetle horns. PNAS 106:8992–97 [Google Scholar]
  104. Moczek AP, Rose DJ, Sewell W, Kesselring BR. 103.  2006. Conservation, innovation, and the evolution of horned beetle diversity. Dev. Genes Evol. 216:655–65 [Google Scholar]
  105. Molkentin JD, Lin Q, Duncan SA, Olson EN. 104.  1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061–72 [Google Scholar]
  106. Morgan TH, Bridges CB. 105.  1916. Sex-Linked Inheritance in Drosophila Carnegie Inst. Wash. Publ. 237 Washington, DC: Carnegie Inst. Wash.
  107. Ng CS, Hamilton AM, Frank A, Barmina O, Kopp A. 106.  2008. Genetic basis of sex-specific color pattern variation in Drosophila malerkotliana. Genetics 180:421–29 [Google Scholar]
  108. Nusslein-Volhard C, Wieschaus E, Kluding H. 107.  1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Roux's Arch. Dev. Biol. 193:267–82 [Google Scholar]
  109. Oliveri P, Tu Q, Davidson EH. 108.  2008. Global regulatory logic for specification of an embryonic cell lineage. PNAS 105:5955–62 [Google Scholar]
  110. Ordway AJ, Hancuch KN, Johnson W, Wiliams TM, Rebeiz M. 109.  2014. The expansion of body coloration involves coordinated evolution in cis and trans within the pigmentation regulatory network of Drosophila prostipennis. Dev. Biol. 392:431–440 [Google Scholar]
  111. Panganiban G, Irvine SM, Lowe C, Roehl H, Corley LS. 110.  et al. 1997. The origin and evolution of animal appendages. PNAS 94:5162–66 [Google Scholar]
  112. Papa R, Morrison CM, Walters JR, Counterman BA, Chen R. 111.  et al. 2008. Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies. BMC Genomics 9:345 [Google Scholar]
  113. Pavlopoulos A, Kontarakis Z, Liubicich DM, Serano JM, Akam M. 112.  et al. 2009. Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean. PNAS 106:13897–902 [Google Scholar]
  114. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA. 113.  et al. 2006. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444:499–502 [Google Scholar]
  115. Peter IS, Davidson EH. 114.  2010. The endoderm gene regulatory network in sea urchin embryos up to mid-blastula stage. Dev. Biol. 340:188–99 [Google Scholar]
  116. Peter IS, Davidson EH. 115.  2011. A gene regulatory network controlling the embryonic specification of endoderm. Nature 474:635–39 [Google Scholar]
  117. Pires-daSilva A, Sommer RJ. 115a.  2003. The evolution of signalling pathways in animal development. Nat. Rev. Genet. 4:39–49 [Google Scholar]
  118. Pisani D, Feuda R, Peterson KJ, Smith AB. 116.  2012. Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships. Mol. Phylogenet. Evol. 62:27–34 [Google Scholar]
  119. Pollard KS, Salama SR, King B, Kern AD, Dreszer T. 117.  et al. 2006. Forces shaping the fastest evolving regions in the human genome. PLOS Genet. 2:e168 [Google Scholar]
  120. Pollard KS, Salama SR, Lambert N, Lambot M-A, Coppens S. 118.  et al. 2006. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443:167–72 [Google Scholar]
  121. Pool JE, Aquadro CF. 119.  2007. The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol. Ecol. 16:2844–51 [Google Scholar]
  122. Prabhakar S, Noonan JP, Pääbo S, Rubin EM. 120.  2006. Accelerated evolution of conserved noncoding sequences in humans. Science 314:786 [Google Scholar]
  123. Prabhakar S, Visel A, Akiyama JA, Shoukry M, Lewis KD. 121.  et al. 2008. Human-specific gain of function in a developmental enhancer. Science 321:1346–50 [Google Scholar]
  124. Quiring R, Walldorf U, Kloter U, Gehring WJ. 122.  1994. Homology of the eyeless gene of Drosophila to the Small eye gene in mice and aniridia in humans. Science 265:785–89 [Google Scholar]
  125. Rafiq K, Cheers MS, Ettensohn CA. 123.  2012. The genomic regulatory control of skeletal morphogenesis in the sea urchin. Development 139:579–90 [Google Scholar]
  126. Range R, Lapraz F, Quirin M, Marro S, Besnardeau L, Lepage T. 124.  2007. Cis-regulatory analysis of nodal and maternal control of dorsal-ventral axis formation by Univin, a TGF-β related to Vg1. Development 134:3649–64 [Google Scholar]
  127. Rebeiz M, Castro B, Liu F, Yue F, Posakony JW. 125.  2012. Ancestral and conserved cis-regulatory architectures in developmental control genes. Dev. Biol. 362:282–94 [Google Scholar]
  128. Rebeiz M, Jikomes N, Kassner VA, Carroll SB. 126.  2011. The evolutionary origin of a novel gene expression pattern through co-option of the latent activities of existing regulatory sequences. PNAS 108:10036 [Google Scholar]
  129. Rebeiz M, Stone T, Posakony JW. 127.  2005. An ancient transcriptional regulatory linkage. Dev. Biol. 281:299–308 [Google Scholar]
  130. Rebeiz M, Williams TM. 128.  2011. Experimental approaches to evaluate the contributions of candidate cis-regulatory mutations to phenotypic evolution. Methods Mol. Biol. 772:351–75 [Google Scholar]
  131. Reed RD, Papa R, Martin A, Hines HM, Counterman BA. 129.  et al. 2011. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137–41 [Google Scholar]
  132. Ronshaugen M, McGinnis N, McGinnis W. 130.  2002. Hox protein mutation and macroevolution of the insect body plan. Nature 415:914–17 [Google Scholar]
  133. Röttinger E, Croce J, Lhomond G, Besnardeau L, Gache C, Lepage T. 131.  2006. Nemo-like kinase (NLK) acts downstream of Notch/Delta signalling to downregulate TCF during mesoderm induction in the sea urchin embryo. Development 133:4341–53 [Google Scholar]
  134. Royo JL, Maeso I, Irimia M, Gao F, Peter IS. 132.  et al. 2011. Transphyletic conservation of developmental regulatory state in animal evolution. PNAS 108:14186–91 [Google Scholar]
  135. Schreiweis C, Bornschein U, Burguiere E, Kerimoglu C, Schreiter S. 133.  et al. 2014. Humanized Foxp2 accelerates learning by enhancing transitions from declarative to procedural performance. PNAS 111:14253–58 [Google Scholar]
  136. Sethi AJ, Wikramanayake RM, Angerer RC, Range RC, Angerer LM. 134.  2012. Sequential signaling crosstalk regulates endomesoderm segregation in sea urchin embryos. Science 335:590–93 [Google Scholar]
  137. Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS. 135.  et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717–23 [Google Scholar]
  138. Shibata Y, Sheffield NC, Fedrigo O, Babbitt CC, Wortham M. 136.  et al. 2012. Extensive evolutionary changes in regulatory element activity during human origins are associated with altered gene expression and positive selection. PLOS Genet. 8:e1002789 [Google Scholar]
  139. Slack J. 137.  1984. A Rosetta stone for pattern formation in animals?. Nature 310:364–65 [Google Scholar]
  140. Small S, Blair A, Levine M. 138.  1992. Regulation of even-skipped stripe 2 in the Drosophila embryo. EMBO J. 11:4047–57 [Google Scholar]
  141. Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier MEA. 139.  et al. 2010. The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466:720–26 [Google Scholar]
  142. St. Johnston D, Driever W, Berleth T, Richstein S, Nüsslein-Volhard C. 140.  1989. Multiple steps in the localization of bicoid RNA to the anterior pole of the Drosophila oocyte. Development 107:Suppl.13–19 [Google Scholar]
  143. Stern DL. 141.  1998. A role of Ultrabithorax in morphological differences between Drosophila species. Nature 396:463–66 [Google Scholar]
  144. Studer A, Zhao Q, Ross-Ibarra J, Doebley J. 142.  2011. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat. Genet. 43:1160–63 [Google Scholar]
  145. Sucena E, Delon I, Jones I, Payre F, Stern DL. 143.  2003. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 424:935–38 [Google Scholar]
  146. Swanson CI, Schwimmer DB, Barolo S. 144.  2011. Rapid evolutionary rewiring of a structurally constrained eye enhancer. Curr. Biol. 21:1186–96 [Google Scholar]
  147. Tagle DA, Koop BF, Goodman M, Slightom JL, Hess DL, Jones RT. 145.  1988. Embryonic epsilon and gamma globin genes of a prosimian primate (Galago crassicaudatus): nucleotide and amino acid sequences, developmental regulation and phylogenetic footprints. J. Mol. Biol. 203:439–55 [Google Scholar]
  148. Takahashi A, Takahashi K, Ueda R, Takano-Shimizu T. 146.  2007. Natural variation of ebony gene controlling thoracic pigmentation in Drosophila melanogaster. Genetics 177:1233–37 [Google Scholar]
  149. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, Babbitt CC. 147.  et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39:31–40 [Google Scholar]
  150. Tobler A, Kapan D, Flanagan NS, Gonzalez C, Peterson E. 148.  et al. 2005. First-generation linkage map of the warningly colored butterfly Heliconius erato. Heredity 94:408–17 [Google Scholar]
  151. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD. 149.  et al. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40:158–60 [Google Scholar]
  152. Walter MF, Black BC, Afshar G, Kermabon AY, Wright TR, Biessmann H. 150.  1991. Temporal and spatial expression of the yellow gene in correlation with cuticle formation and DOPA decarboxylase activity in Drosophila development. Dev. Biol. 147:32–45 [Google Scholar]
  153. Wang VY, Hassan BA, Bellen HJ, Zoghbi HY. 151.  2002. Drosophila atonal fully rescues the phenotype of Math1 null mice: new functions evolve in new cellular contexts. Curr. Biol. 12:1611–16 [Google Scholar]
  154. Williams TM, Selegue JE, Werner T, Gompel N, Kopp A, Carroll SB. 152.  2008. The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134:610–23 [Google Scholar]
  155. Wittkopp PJ. 153.  2005. Genomic sources of regulatory variation in cis and in trans. Cell. Mol. Life Sci. 62:1779–83 [Google Scholar]
  156. Wittkopp PJ, Carroll SB, Kopp A. 154.  2003. Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet. 19:495–504 [Google Scholar]
  157. Wittkopp PJ, Vaccaro K, Carroll SB. 155.  2002. Evolution of yellow gene regulation and pigmentation in Drosophila. Curr. Biol. 12:1547–56 [Google Scholar]
  158. Wittkopp PJ, Williams BL, Selegue JE, Carroll SB. 156.  2003. Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes. PNAS 100:1808–13 [Google Scholar]
  159. Wray GA. 157.  2007. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 8:206–16 [Google Scholar]
  160. Wright S. 158.  1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the Sixth International Congress on Genetics 1 Transactions and General Addresses DF Jones 356–66 Austin, TX: Genet. Soc. Am.
  161. Yeh S-D, Liou S-R, True JR. 159.  2006. Genetics of divergence in male wing pigmentation and courtship behavior between Drosophila elegans and D. gunungcola. Heredity 96:383–95 [Google Scholar]
  162. Yuh C-H, Brown CT, Livi CB, Rowen L, Clarke PJC, Davidson EH. 160.  2002. Patchy interspecific sequence similarities efficiently identify positive cis-regulatory elements in the sea urchin. Dev. Biol. 246:148–61 [Google Scholar]
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